Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion

Georgia F Symons; Meaghan Clough; Steven Mutimer; Brendan P Major; William T O'Brien; Daniel Costello; Stuart J McDonald; Zhibin Chen; Owen White; Richelle Mychasiuk; Meng Law; David K Wright; Terence J O'Brien; Joanne Fielding; Scott C Kolbe; Sandy R Shultz

doi:10.1093/braincomms/fcab213

Cognitive ocular motor deficits and white matter damage chronically after sports-related concussion

Brain Commun. 2021 Sep 14;3(3):fcab213. doi: 10.1093/braincomms/fcab213. eCollection 2021.

Authors

Georgia F Symons¹, Meaghan Clough¹, Steven Mutimer², Brendan P Major¹, William T O'Brien¹, Daniel Costello², Stuart J McDonald¹, Zhibin Chen¹, Owen White^{1

2}, Richelle Mychasiuk¹, Meng Law¹, David K Wright¹, Terence J O'Brien^{1

2}, Joanne Fielding^{1

2}, Scott C Kolbe¹, Sandy R Shultz^{1

2}

Affiliations

¹ Department of Neuroscience, Central Clinical School, Monash University, Melbourne, Australia.
² Department of Medicine, Royal Melbourne Hospital, University of Melbourne, Parkville, Australia.

Abstract

A history of concussion has been linked to long-term cognitive deficits; however, the neural underpinnings of these abnormalities are poorly understood. This study recruited 26 asymptomatic male Australian footballers with a remote history of concussion (i.e. at least six months since last concussion), and 23 non-collision sport athlete controls with no history of concussion. Participants completed three ocular motor tasks (prosaccade, antisaccade and a cognitively complex switch task) to assess processing speed, inhibitory control and cognitive flexibility, respectively. Diffusion tensor imaging data were acquired using a 3 T MRI scanner, and analysed using tract-based spatial statistics, to investigate white matter abnormalities and how they relate to ocular motor performance. Australian footballers had significantly slower adjusted antisaccade latencies compared to controls (P = 0.035). A significant switch cost (i.e. switch trial error > repeat trial error) was also found on the switch task, with Australian footballers performing increased magnitude of errors on prosaccade switch trials relative to prosaccade repeat trials (P = 0.023). Diffusion tensor imaging analysis found decreased fractional anisotropy, a marker of white matter damage, in major white matter tracts (i.e. corpus callosum, corticospinal tract) in Australian footballers relative to controls. Notably, a larger prosaccade switch cost was significantly related to reduced fractional anisotropy in anterior white matter regions found to connect to the prefrontal cortex (i.e. a key cortical ocular motor centre involved in executive functioning and task switching). Taken together, Australian footballers with a history of concussion have ocular motor deficits indicative of poorer cognitive processing speed and cognitive flexibility, which are related to reduce white matter integrity in regions projecting to important cognitive ocular motor structures. These findings provide novel insights into the neural mechanisms that may underly chronic cognitive impairments in individuals with a history of concussion.

Keywords: MRI; biomarker; cognition; diffuse axonal injury; mild traumatic brain injury.